Nota Cuad. herpetol. 35 (1): 177-181 (2021) Distribution extension of Amphisbaena lumbricalis Vanzolini, 1996 with its first predation record by snakeErythrolamprus viridis (Günther, 1862) Ana Paula Gomes Tavares1, Alcéster Diego Coelho-Lima2, Fagner Ribeiro Delfim3, Daniel Oliveira Mesquita3, Daniel Cunha Passos2,4 1 Universidade Federal Rural de Pernambuco – UFRPE, Programa de Pós-Graduação em Ecologia, Laboratório de Estudos Herpetológicos e Paleoherpetológicos, Recife, Pernambuco, Brasil. 2 Universidade Federal Rural do Semi-Árido – UFERSA, Programa de Pós-Graduação em Ecologia e Conser- vação, Laboratório de Ecologia e Comportamento Animal, Mossoró, Rio Grande do Norte, Brasil. 3 Universidade Federal da Paraíba – UFPB, Centro de Ciências Exatas e da Natureza, Departamento de Siste- mática e Ecologia, João Pessoa, Paraíba, Brasil. 4 Universidade Federal Rural do Semi-Árido – UFERSA, Centro de Ciências Biológicas e da Saúde, Departa- mento de Biociências, Mossoró, Rio Grande do Norte, Brasil.
Recibida: 25 Septiembre 2020 ABSTRACT Revisada: 12 Octubre 2020 We expand the geographical distribution of Amphisbaena lumbricalis throughout the first record Aceptada: 11 Diciembre 2020 for a semiarid Caatinga area in the Paraíba state, northeastern Brazil. Furthermore, we report Editor Asociado: J. Goldberg the first predation report of A. lumbricalis by the snake Erythrolamprus viridis. Our findings contribute with information about the habitats occupied by a hitherto considered “Data Defi- cient” species, beyond to reveal the potential of E. viridis to prey upon reptiles. doi: 10.31017/CdH.2021.(2020-068) Key Words: Geographical Distribution; Predator-Prey Interaction; Caatinga.
Data on geographic distribution is essential to sub-Saharan Africa, parts of the Mediterranean support conservation actions and effective species region, Baja California, and Florida (Vitt and Cald- management. Although representing about 20% of well, 2014; Longrich et al., 2015; Uetz et al., 2020). the world’s reptiles and amphibians, the fossorial Amphisbaenidae, the most diverse family (ca. 170 herpetofauna is still poorly known (Measey, 2006). species), is distributed throughout South America Fossorial reptiles have received relatively little atten- and Africa (Gans, 2005; Vidal et al., 2008; Uetz et al., tion, and the lack of knowledge about these animals 2020). Around 40% (80 species) of all amphisbaenids is usually attributed to their secretive habits, which occur in Brazil, and 27 species along the semiarid leads to several sampling difficulties (Frey, 2006; Caatinga (Almeida et al., 2018; Costa and Bérnils, Filho et al., 2013). Amphisbaenia is one of the major 2018; Ribeiro et al., 2018, Uetz et al., 2020). groups of fossorial reptiles, and like any secretive Amphisbaena lumbricalis Vanzolini, 1996 was species, studies on several aspects, such as natural described to the Xingó Hydroelectric Power Plant history, ecology, and distribution, are still scarce located in the lower São Francisco River, which divi- (Pearse and Pogson, 2000; Macey et al., 2004). des the states of Alagoas and Sergipe in the Northeast Currently, Amphisbaenia congregates appro- region from Brazil (Vanzolini, 1996). Initially, its ximately 200 described species, from six families distribution was in Delmiro Gouveia and Piranhas’s (Amphisbaenidae, Bipedidae, Blanidae, Cadeidae, municipalities in Alagoas state, and in Canindé de Rhineuridae, and Trogonophidae) with a wide geo- São Francisco in Sergipe state (Vanzolini, 1996). In graphical distribution, since the Neotropical region, 2015, it was recorded for Traipu municipality in Ala- Author for correspondenc: [email protected] 177 A. P. Gomes Tavares et al. - Distribution extension of A. lumbricalis. goas state (100 km to its southeast site), in an ecotone ning gut contents of a specimen of Erythrolamprus between Atlantic Forest and Caatinga environments, viridis housed in the herpetological collection of including a non-sandy area (Galdino et al., 2015). the Universidade Federal da Paraíba – CHUFPB. Subsequently, it was extended to the Pernambuco The predator (CHUFPB 17237) was an adult male state, for the municipalities of Custódia, Floresta and with 403 mm of snout-vent length collected at São Sertânia associated with several soil types (Tavares Mamede municipality, Paraíba state (Fig. 1). The et al., 2017). The last distribution update was recor- predator’s identity was determined by a combination ded to the Reserva Biológica Guaribas (hereafter of following meristic characters: 19/19/17 dorsal, REBIO Guaribas) in the Mamanguape municipality, 185 ventral, divided subcaudal, and eight supralabial Paraíba state, an integral protection unit inserted in scales. The prey consisted in the anterior region the Atlantic Forest domain (Mesquita et al., 2018). of an individual of A. lumbricalis with 57.2 mm of Herein, we expand the geographical distribution length, and 3.2 mm of diameter, which was housed of A. lumbricalis throughout the first record for a in the scientific collection Coleção Herpetológica Caatinga area in the Paraíba state, beyond to report do Semiárido – CHSA at Universidade Federal Ru- the first predation case of A. lumbricalis by the snake ral do Semi-Árido. Despite this material (CHSA R Erythrolamprus viridis (Günther, 1862). 1714) was in an advanced degree of deterioration, During a snake ecology study in several her- we were able to precisely identify the target species petological collections in the northeastern Brazil, by its slender body diameter and typical cephalic we found one specimen of A. lumbricalis in exami- scutelation. In comparison with other slender am-
Figure 1. Updated distribution map of Amphisbaena lumbricalis. Black star constitutes the new record to São Mamede municipality in Paraíba state. Colorful symbols correspond to the previously known records: yellow diamond (type-locality; Xingó - Alagoas; Vanzolini, 1996), red triangles (Delmiro Gouveia, Piranhas and Traipu - Alagoas; Canindé do São Francisco - Sergipe; Galdino et al., 2015), blue circles (Custódia, Floresta, Sertânia - Pernambuco; Tavares et al., 2017), and green square (Mamanguape - Paraíba; Mesquita et al., 2018). Caatinga ecoregions follows Silva et al. (2017).
178 Cuad. herpetol. 36 (1): 177-181 (2021) phisbaenian species, the size and shape of posterior distinguish A. lumbricalis from A. carvalhoi Gans, edge of frontal scales allow to distinguish A. lum- 1965 (smaller and shorter prefrontal scales). bricalis from A. hastata Vanzolini, 1991 (greater Our record of A. lumbricalis to São Mamede angle between two smaller frontal scales) and A. municipality in Paraíba state extends its distribu- heathi Schmidt, 1936 (smaller angle between two tion (Fig. 1, Table 1) by 134 km Northeast from larger frontal scales); the shape of anterior edge of the nearest previously recorded locality (Sertânia frontal scales allows to distinguish A. lumbricalis municipality, Pernambuco state), and by 217 km from A. ignatiana Vanzolini, 1991 (arched anterior W from the northeast known occurrence site (Ma- edge and greater angle between two frontal scales); manguape municipality, Paraíba state). This latter and the size and shape of prefrontal scales allow to was the first record of A. lumbricalis to Paraíba state,
Table 1. Detailed information of all known geographical records of Amphisbaena lumbricalis. Acronyms: CHSAR - Coleção Her- petológica do Semiárido, MFCH - Coleção de Herpetologia do Museu de Fauna da Caatinga, MUFAL - Museu de História Natural da Universidade Federal de Alagoas, MZUSP - Museu de Zoologia da Universidade de São Paulo, and RT Coleção Herpetológica da Universidade Federal da Paraíba em Rio Tinto. Municipality State Ecoregion Latitude Longitude Voucher Source Hydroelectric of Xingó, on the left MZUSP 79433 Depressão Sertaneja bank of the Rio São Alagoas -9.400 -37.967 MZUSP 79434-79490 Vanzolini, 1996 Meridional Francisco (type MZUSP 79419-79432 locality) Depressão Sertaneja Galdino et al., Delmiro Gouveia Alagoas -9.386 -37.997 MUFAL 2790 Meridional 2015 MUFAL 2785, 2786, Depressão Sertaneja Galdino et al., Piranhas Alagoas -9.600 -37.759 2787, 2802, 2803, Meridional 2015 2804, 2805; 2493 Depressão Sertaneja Galdino et al., Traipu Alagoas -9.759 -36.948 MUFAL 9071; 9812 Meridional 2015 MUFAL 2777; 2778; 2779; 2780; 2781; 2782; 2783; 2784; 2789; 2796; 2797; Canindé do São Depressão Sertaneja Galdino et al., Sergipe -9.642 -37.789 2798; 2800; 2806; Francisco Meridional 2015 2807; 2808; 2809; 2811; 2812; 2813; 2814; 2815; 2816; 2817; 2818; 2819 Depressão Sertaneja Custódia Pernambuco -8.237 -37.655 MFCH 2183 Tavares et al., 2017 Meridional Floresta Pernambuco Raso da Catarina -8.624 -38.137 MFCH 2180 Tavares et al., 2017 Depressão Sertaneja Sertânia Pernambuco -8.109 -37.404 MFCH 2163 Tavares et al., 2017 Meridional Mesquita et al., Mamanguape Paraíba Atlantic Forest -6.742 -35.142 RT 0267 2018 Depressão Sertaneja São Mamede Paraíba -6.932 -37.097 CHSAR 1714 Present study Setentrional in the REBIO Guaribas, despite there is no detailed and Vieira, 2017; Costa-Lima and Alves, 2018), as information on the habitat in which voucher speci- the Tabuleiros, and Stational Semidecidual Forest mens were collected (Mesquita et al. 2018). However, (Oliveira-Filho and Carvalho, 1993; Mesquita et al., REBIO Guaribas is inserted in the Atlantic Forest 2018). Therefore, our findings constitute the second domain, including complex vegetation formations record of A. lumbricalis for the Paraíba state and the throughout its range (Barbosa et al., 2011; Melo first record for the semiarid Caatinga in this state.
179 Cuad. herpetol. 36 (1): 177-181 (2021)
This new site is a typical Caatinga area located in research fellowship (proc. 306541/2017-3). the Depressão Sertaneja Setentrional ecoregion (Fig. 1, Table 1), constituted by hyperoxerophilous Literature cited vegetation and deciduous forest patches. Thus, we Almeida, J.P.F.A.; Freitas, M.A.; Silva, M.B.; Valverde, M.C.C.; contributed with information about the mesohabi- Rodrigues, M.T.; Pires, A. M. & Mott, T. 2018. A new four- pored Amphisbaena (Squamata: Amphisbaenidae) from tats occupied by A. lumbricalis, which still remains northeastern Brazil. Zootaxa 4514: 553-562. categorized as “Data Deficient “ for conservation Barbo, F.E. & Marques, O.A.V. 2003. Do aglyphous colubrid purposes (Mott, 2010). snakes prey on live amphisbaenids able to bite? Phyllomedusa Regarding the predation record, the genus 2: 113-114. Erythrolamprus belongs to an anuran-eating snakes Barbosa, M.R.V.; Thomas, W.W.; Zárate, E.L.P.; Lima, R.B.; Agra, M.F.; Lima, I.B.; Pessoa, M.C.R.; Lourenco, A.R.L.; guild, whose the most species from Caatinga can Delgado Junior, G.C.; Pontes, R.A.S.; Chagas, E.C.O.; Viana, be considered anuran specialists (Vitt, 1983). One J.L.; Gadelha Neto, P.C.; Araújo, C.M.L.R.; Araújo, A.A.M.; of them is Erythrolamprus viridis, a small diurnal Freitas, G.B.; Lima, J.R.; Silva, F.O.; Vieira, L.A.F.; Pereira, and terrestrial snake whose ecology remains poorly L.A.; Costa, R.M.T.; Duré, R.C. & Sá, M.G.V. 2011. Checklist studied. A pioneering study described that E. vi- of the Vascular Plants of the Guaribas Biological Reserve, Paraíba, Brazil. Revista Nordestina de Biologia 20: 79-106. ridis feed on frogs, treefrogs, and toads (Vitt and Caramaschi, U. & Niemeyer, H. 2012. Unsuccessful Vangilder, 1983), but recently, it was recorded that predation of Elapomorphus quinquelineatus (Serpentes: it can also prey lizards (Mesquita et al., 2013). An Colubridae) on Amphisbaena microcephala (Amphisbaenia: Amphisbaena recorded in the digestive tract of E. Amphisbaenidae). Herpetology Notes 5: 429-430. viridis expands its prey list, reinforcing its ability to Cisneros-Heredia, D.F. 2005. Predation upon Amphisbaena preying reptiles. Although this event might be con- fuliginosa LINNAEUS, 1758 by Micrurus ancoralis (JAN, 1872). Herpetozoa 18: 93-94. sidered fortuitous, further studies on ecology of E. Costa, H.C. & Bérnils, R.S. 2018. Répteis do Brasil e suas viridis are required to a better understanding of its unidades federativas: lista de espécies. Herpetologia dietary preferences. However, due to their secretive Brasileira 7: 11-57. habits, these occasions provide a unique opportunity Costa-Lima, J.L. & Alves, M. 2018. Flora da Reserva Biológica to acquire natural history data on such species guild. Guaribas, Estado da Paraíba, Brasil: Erythroxylaceae. Hoehnea 45(3): 372-378. Despite its fossorial habits, amphisbaenians Dixon, J. 1989. Prey items of 20 species of the neotropical are preyed by a sort of predators, as such as many colubrid snake genus Liophis. Herpetological Review 20: birds (Folly et al., 2015; Hayes et al., 2015), mam- 139-141. mals (Oliveira et al., 2004; Soibelzon et al., 2007) and Duarte, M.R. 2006. Phalotris mertensi (False coral snake) and snakes (Marques and Sazima, 1997; Maschio et al., Amphisbaena mertensi (NCN). Predation. Herpetological 2010). Many fossorial snakes commonly prey on am- Review 37: 234. phisbaenians, like elapids (Zamprogno and Sazima, Filho, J.D.B.; Freitas, M.A.; Silva, T.F.S.; Valverde, M.C.C.; Loguercio, M.F.C. & Veríssimo, D. 2013. On the Distribution 1993; Cisneros-Heredia, 2005) and Elapomorphini and Habitat of Leposternon octostegum (Duméril, 1851) species (Duarte, 2006; Caramaschi and Niemeyer, (Squamata: Amphisbaenidae). Wildlife Biology in Practice 2012). However, the consumption of worm lizards 9: 1-6. by terrestrial snakes is much scarcer. Dixon (1989) Folly, H.; Neves, M.O.; Pereira, E.A.; Hote, P.; Souza, R.A. & reported this behavior for the Xenodontini Eryth- Santana, D.J. 2015. Predation on Leposternon microcephalum (Squamata, Amphisbaenidae) by Cariama cristata rolamprus poecilogyrus (Wied-Neuwied, 1825) and (Cariamiformes, Cariamidae). Herpetology Notes 8: 465-466. Barbo and Marques (2003) for the Echinantherini Frey, J. K. 2006. Inferring species distributions in the absence Taeniophallus affinis (Günther, 1858). Our finding of occurrence records: An example considering wolverine for E. viridis reveals its potential on preying amphis- (Gulo gulo) and Canada lynx (Lynx canadensis) in New baenians, allowing us to consider that this behavior is Mexico. Biological conservation 30: 16-24. Galdino, J. Y.; Gonçalves, U.; Matias, G. & Torquato, S. 2015. less rare than expected between Xenodontini snakes. Amphisbaena lumbricalis Vanzolini, 1996 (Squamata: Amphisbaenidae). Distribution extension and map. Boletim Acknowledgments do Museu de Biologia Mello Leitão 37: 293-299. APGT thanks FACEPE, through the granting of Gans, C. 2005. Checklist and Bibliography of the Amphisbaenia a postgraduate scholarship (masters) IBPG-0108- of the World. Bulletin of the American Museum of Natural History 289: 1-130. 2.05/18. ADCL thanks FAPERN and CAPES (Fi- Hayes, F.E.; Capllonch, P. & Montero, R. 2015. Predation on nance Code – 001) for providing a postgraduate Amphisbaena heterozonata (Squamata: Amphisbaenidae) (masters) scholarship. DOM thanks CNPq for the by the whistling heron Syrigma sibilatrix (Pelecaniformes:
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